Metatranscriptomics reveals a differential temperature effect on the structural and functional organization of the anaerobic food web in rice field soil

Abstract

BackgroundThe expected increase in global surface temperature due to climate change may have a tremendous effect on the structure and function of the anaerobic food web in flooded rice field soil. Here, we used the metatranscriptomic analysis of total RNA to gain a system-level understanding of this temperature effect on the methanogenic food web.ResultsMesophilic (30 °C) and thermophilic (45 °C) food web communities had a modular structure. Family-specific rRNA dynamics indicated that each network module represents a particular function within the food webs. Temperature had a differential effect on all the functional activities, including polymer hydrolysis, syntrophic oxidation of key intermediates, and methanogenesis. This was further evidenced by the temporal expression patterns of total bacterial and archaeal mRNA and of transcripts encoding carbohydrate-active enzymes (CAZymes). At 30 °C, various bacterial phyla contributed to polymer hydrolysis, with Firmicutes decreasing and non-Firmicutes (e.g., Bacteroidetes, Ignavibacteriae) increasing with incubation time. At 45 °C, CAZyme expression was solely dominated by the Firmicutes but, depending on polymer and incubation time, varied on family level. The structural and functional community dynamics corresponded well to process measurements (acetate, propionate, methane). At both temperatures, a major change in food web functionality was linked to the transition from the early to late stage. The mesophilic food web was characterized by gradual polymer breakdown that governed acetoclastic methanogenesis (Methanosarcinaceae) and, with polymer hydrolysis becoming the rate-limiting step, syntrophic propionate oxidation (Christensenellaceae, Peptococcaceae). The thermophilic food web had two activity stages characterized first by polymer hydrolysis and followed by syntrophic oxidation of acetate (Thermoanaerobacteraceae, Heliobacteriaceae, clade OPB54). Hydrogenotrophic Methanocellaceae were the syntrophic methanogen partner, but their population structure differed between the temperatures. Thermophilic temperature promoted proliferation of a new Methanocella ecotype.ConclusionsTemperature had a differential effect on the structural and functional continuum in which the methanogenic food web operates. This temperature-induced change in food web functionality may not only be a near-future scenario for rice paddies but also for natural wetlands in the tropics and subtropics.Electronic supplementary materialThe online version of this article (10.1186/s40168-018-0546-9) contains supplementary material, which is available to authorized users.

Temperature-Dependent Network Modules of Soil Methanogenic Bacterial and Archaeal Communities

“…The functions of these different taxa within the methanogenic degradation process are unclear, but most probably involve various hydrolytic and fermentation processes. Helicobacteraceae , for example, may be involved in anaerobic oxidation of propionate, possibly even acetate ( Noll et al, 2010 ; Sattley and Madigan, 2014 ; Liu et al, 2018 ; Peng et al, 2018 ). The different bacterial taxa were separated together with archaeal taxa into three major network modules, the most distinct being those in soils exposed to 45°C versus those exposed to moderate temperatures (either 25 or 35°C).…”

“…This change often coincides with a change in the methanogenic pathway from a mixture of acetoclastic plus hydrogenotrophic to exclusively hydrogenotrophic methanogenesis, and by the replacement of acetoclastic methanogenesis by syntrophic acetate oxidation that is coupled to hydrogenotrophic methanogenesis ( Conrad et al, 2009 ; Liu and Conrad, 2010 ; Rui et al, 2011 ). Recently, metatranscriptomics and co-occurrence network analysis revealed that the microbial community of Italian rice field soil consisted of modules characterized by the functional activities of polymer hydrolysis, syntrophic oxidation of key intermediates, and methanogenesis ( Peng et al, 2018 ). Both mesophilic (30°C) and moderate thermophilic (45°C) temperatures had a differential effect on all the functional activities ( Peng et al, 2018 ).…”

“…Recently, metatranscriptomics and co-occurrence network analysis revealed that the microbial community of Italian rice field soil consisted of modules characterized by the functional activities of polymer hydrolysis, syntrophic oxidation of key intermediates, and methanogenesis ( Peng et al, 2018 ). Both mesophilic (30°C) and moderate thermophilic (45°C) temperatures had a differential effect on all the functional activities ( Peng et al, 2018 ).…”

Microbial Resource Management for Ex Situ Biomethanation of Hydrogen at Alkaline pH

“…The acetate consumption could have occurred via SAO (e.g., by members of the classes Synergistia or OPB54 (Firmicutes) [60]), or could have been assimilated by acetogens and hydrogenotrophic methanogens to build biomass. The order Thermoanaerobacterales (class Clostridia) was present in lower abundance (3% in T6), with its dynamic behavior in the second stage reaching similar levels as in the inoculum.…”

Development and Analysis of a Stable, Reduced Complexity Model Soil Microbiome

“…However, not all genes are expressed at any given time, and DNA extracted from soil can also represent dormant, or dead, populations that are not contributing to any given function. The soil metatranscriptome has been used to determine functions that are expressed by members of the soil microbiome ( Tveit et al, 2014 ; Hultman et al, 2015 ; Jiang et al, 2016 ; Peng et al, 2018 ; Roy Chowdhury et al, 2019 ). However, these studies generally rely on relatively shallow metatranscriptomes, with a read depth that is insufficient to cover all the members of the community and therefore only queries the most abundant and transcriptionally active species and genes.…”